Elsevier

Food Control

Volume 21, Issue 4, April 2010, Pages 370-380
Food Control

Review
Lactic acid bacteria – Potential for control of mould growth and mycotoxins: A review

https://doi.org/10.1016/j.foodcont.2009.07.011Get rights and content

Abstract

Most data dealing with the biopreservative activity of lactic acid bacteria (LAB) are focused on their antibacterial effects. Food spoilage by mould and the occurrence of their mycotoxins constitute a potential health hazard. Development of biological control should help improve the safety of products by controlling mycotoxin contamination. Data have actually shown that many LAB can inhibit mould growth and that some of them have the potential to interact with mycotoxins.

This review summarizes these findings and demonstrates that LAB are promising biological agents for food safety.

Introduction

Mycotoxinogenic moulds such as Aspergillus, Fusarium and Penicillium play an undeniable role in the deterioration of the marketable quality and hygiene of foodstuffs by synthesizing highly toxic metabolites known as mycotoxins. Several of these toxins have been identified but quite a few could be responsible for significant problems in foodstuffs. Six classes of mycotoxins are frequently encountered in different food systems: aflatoxins, fumonisins, ochratoxins, patulin, trichothecenes and zearalenone. Concerning the importance and diversity of their toxic effects - carcinogenic, immunotoxic, teratogenic, neurotoxic, nephrotoxic and hepatotoxic - the occurrence of mycotoxinogenic moulds in foods is potentially dangerous for public health and also constitutes a major economic problem. For example, in Western Europe, the economic losses related to the presence of moulds in bread are estimated to be more than 200 million euros per year (Legan, 1993). Physical and chemical methods have been developed to control the occurrence of these microorganisms and their toxins, but no efficient strategy has yet been proposed to reduce the presence of mycotoxins. Moreover, some moulds have acquired the ability to resist chemical treatments and some preservatives. For example, some Penicillium can grow in the presence of potassium sorbate (Davidson, 2001) and other moulds possess the ability to degrade sorbate (Nielsen & de Boer, 2000). The reduction of such moulds in food production is thus of primary importance and there is great interest in developing efficient and safe strategies for this purpose. Biopreservation, the control of one organism by another, has received much attention in the last ten years (Magnusson, Ström, Roos, Sjögren, & Schnürer, 2003).

Among natural biological antagonists, LAB have several potential applications. These microorganisms are widely used for the production of fermented foods and are also part of intestinal microflora. Research reports indicate that LAB have beneficial health effects in humans. These bacteria have a long history of use in foods. They produce some antagonistic compounds able to control pathogenic bacteria and undesirable spoilage microflora, in particular. Using LAB to control mould growth could be an interesting alternative to physical and chemical methods because these bacteria have been reported to have strong antimicrobial properties. However, the antifungal activity of lactic strains remains to be elucidated. A limited number of reports have shown that a good selection of LAB could allow the control of mould growth and improve the shelf life of many fermented products and, therefore, reduce health risks due to exposure to mycotoxins (Gourama & Bullerman, 1995).

In this review, the ability of LAB to control mycotoxinogenic mould growth, the antifungal substances that have been characterised as of this time and the interactions of these organisms with some mycotoxins are successively investigated.

Section snippets

Lactic acid bacteria are able to control mycotoxinogenic mould growth

Due to their nutritional requirements, LAB are generally cultivated in enriched media and are found in dairy products, meat, meat-derived products and cereal products (Carr, Chill, & Maida, 2002). These bacteria are mainly divided into four genera: Lactococcus, Lactobacillus, Leuconostoc and Pediococcus. They are traditionally used as preservative agents to prevent spoilage and to extend the shelf life of food and feed.

According to Magnusson et al. (2003), three mechanisms may explain the

Factors that influence the antifungal activity of lactic acid bacteria

A well-designed selection of potential antifungal LAB could reduce the problem of toxinogenic moulds. However, relevant use of antifungal LAB requires thorough knowledge of the parameters that modulate their antifungal properties. Numerous parameters have been considered, including temperature, time of incubation, growth medium, pH and nutritional factors (Batish et al., 1997).

Antifungal metabolites produced by lactic acid bacteria

Several compounds with a strong antifungal activity have been isolated from bacterial cultures. As of this time, the majority of identified antifungal substances are low-molecular-weight compounds composed of organic acids, reuterin, hydrogen peroxide, proteinaceous compounds, hydroxyl fatty acids and phenolic compounds (Table 2).

Lactic acid bacteria–mycotoxin interactions

Most data dealing with the effects of LAB on the accumulation of mycotoxins are related to aflatoxin-producing moulds. Wiseman and Marth (1981) revealed the existence of an amensalism relationship between Lc. lactis and A. parasiticus. When these authors added the spores of A. parasiticus to a 13-day-old culture of Lc. lactis, they observed the entire repression of aflatoxin production. When the fungal spore suspension and the lactic strain were inoculated simultaneously, an increase in

Inhibition of mycotoxin biosynthesis by lactic acid bacteria

Several papers dealing with the inhibition of mycotoxin biosynthesis by LAB have focused on aflatoxins (Thyagaraja & Hosono, 1994). During cell lysis, it is possible that LAB releases molecules that potentially inhibit mould growth and therefore lead to a lower accumulation of their mycotoxins (Gourama & Bullerman, 1995). These “anti-mycotoxinogenic” metabolites could also be produced during LAB growth. Gourama (1991), using a dialysis assay, demonstrated the occurrence of a metabolite that

Binding of mycotoxins by lactic acid bacteria

The cell walls of some LAB such as Leuconostoc and Streptococcus have been reported to be able to bind some mutagenic compounds such as amino acid pyrolysates and heterocyclic amino acids produced during cooking. Similar results were obtained with other LAB isolated from fermented products (Rajendran and Ohta, 1998, Thyagaraja and Hosono, 1994). Further investigations have been conducted to evaluate the ability of LAB to remove other food-contaminating substances including mycotoxins, known for

Mechanism of mycotoxin binding by lactic acid bacteria

Few investigations have been conducted to elucidate the mechanism by which some mycotoxins such as aflatoxins, zearalenone and fumonisins are trapped by LAB pellets. It has been demonstrated that when heat or acid treatments were applied to LAB, their ability to remove aflatoxin B1 increased (El-Nezami et al., 1998). According to this result, supplementation of some basic compounds (NaOH and Na2CO3) and isopropanol was shown to negatively influence this binding. Viability of LAB strains was not

Stability of the lactic bacteria–mycotoxin complex

Potential future applications of LAB to reduce mycotoxin availability rely on the relative stability of the complexes formed. In the case of weak binding interactions, mycotoxins may be released by the continual washing of the bacterial surface in the gastrointestinal tract. Several studies have attempted to assess the stability of the complexes formed between mycotoxins and LAB and have concluded that the binding strength significantly depends on the strain and on environmental conditions.

Conclusion

The analysis of data available in the literature dealing with antifungal activity of LAB has highlighted the ability of some strains to repress mycotoxinogenic mould growth through the production of several low-molecular-weight antifungal metabolites. Even if some of these antifungal metabolites, including cyclic dipeptides, phenyllactic acids and 3-hydroxylated fatty acids, have been successfully purified, most of these low-molecular-mass compounds remain to be identified due to the lack of

Acknowledgements

This work is part of Doguiet Dalie’ PhD project financially supported by the “Ministère de l’Enseignement Supérieur et de la Recherche Scientifique” of Côte d’Ivoire, as part of the Integrated Research Project ‘‘Qualité Sanitaire des Aliments en Aquitaine 2006–2008”.

References (86)

  • Y.I. Hassan et al.

    Antifungal activity of Lactobacillus paracasei ssp tolerans isolated from a sourdough bread culture

    International Journal of Food Microbiology

    (2008)
  • P. Kankaanpää et al.

    Binding of aflatoxin B1 alters the adhesion properties of Lactobacillus rhamnosus strain GG in Caco-2 model

    Journal of Food Protection

    (2000)
  • A. Karunaratne et al.

    Inhibition of mold growth and aflatoxin production by Lactobacillus spp

    Journal of Food Protection

    (1990)
  • T.R. Klaenhammer

    Genetics of bacteriocin produced by lactic acid bacteria

    FEMS Microbiology Reviews

    (1993)
  • Y.K. Lee et al.

    Kinetics of adsorption and desorption of aflatoxin B1 by viable and nonviable bacteria

    Journal of Food Protection

    (2003)
  • J.D. Legan

    Mould spoilage of bread: the problem and some solutions

    International Biodeterioration and Biodegradation

    (1993)
  • S. Lindgren et al.

    Antagonistic activities of lactic acid bacteria in food and feed fermentations

    FEMS Microbiology Review

    (1990)
  • J. Magnusson et al.

    Broad and complex antifungal activity among environmental isolates of lactic acid bacteria

    FEMS Microbiology Letters

    (2003)
  • N.S. Reddy et al.

    Nutritional factors affecting growth and production of antimicrobial substance by Streptococcus lactis diacetylactis S1-67-C

    Journal of Food Protection

    (1983)
  • U. Roy et al.

    Production of antifungal substance by Lactococcus lactis subsp. lactis CHD-28.3

    International Journal of Food Microbiology

    (1996)
  • J. Schnürer et al.

    Antifungal lactic acid bacteria as biopreservatives

    Trends in Food Science and Technology

    (2005)
  • H. Schütz et al.

    Anaerobic reduction of glycerol to propanediol-1, 3 by Lactobacillus brevis and Lactobacillus buchneri

    Systematic and Applied Microbiology

    (1984)
  • J. Stiles et al.

    Antifungal activity of sodium acetate and Lactobacillus rhamnosus

    Journal of Food Protection

    (2002)
  • K. Ström et al.

    Co-cultivation of antifungal Lactobacillus plantarum MiLAB 393 and Aspergillus nidulans, evaluation of effects on fungal growth and protein expression

    FEMS Microbiology Letters

    (2005)
  • N. Thyagaraja et al.

    Binding properties of lactic acid bacteria from Idly towards food-borne mutagens

    Food and Chemical Toxicology

    (1994)
  • Axelsson, L. (1990). Lactobacillus reuteri a member of the gut bacterial flora. Ph.D. Thesis, Swedish University of...
  • A.S. Baptista et al.

    The capacity of mano-oligosaccharides thermolysed yeast and active yeast to attenuate aflatoxicosis

    World Journal of Microbiology and Biotechnology

    (2004)
  • V.K. Batish et al.

    Screening lactic acid starter cultures for antifungal activity

    Journal of Cultured and Dairy Products

    (1989)
  • V.K. Batish et al.

    Effect of nutritional factors on the production of antifungal substance by Lactococcus lactis biovar. Diacetylactis

    Australian Journal of Dairy Technology

    (1990)
  • V.K. Batish et al.

    Antifungal attributes of lactic acid bacteria – A review

    Critical Reviews in Biotechnology

    (1997)
  • A. Broberg et al.

    Metabolite profiles of lactic acid bacteria in grass silage

    Applied and Environmental Microbiology

    (2007)
  • D.J. Bueno et al.

    Physical Adsorption of Aflatoxin B1 by lactic acid bacteria and Saccharomyces cerevisiae: A theoretical model

    Journal of Food Protection

    (2006)
  • F.J. Carr et al.

    The lactic acid bacteria: A literature survey

    Critical Reviews in Microbiology

    (2002)
  • T.C. Chung et al.

    In vitro studies on reuterin synthesis by Lactobacillus reuteri

    Microbial Ecology and Health and Disease

    (1989)
  • J. Coallier-Ascah et al.

    Interaction between Streptococcus lactis and Aspergillus flavus on production of aflatoxin

    Applied and Environmental Microbiology

    (1985)
  • A. Corsetti et al.

    Antimould activity of sourdough lactic acid bacteria: identification of a mixture of organic acids produced by Lactobacillus sanfrancisco CB1

    Applied Microbiology and Biotechnology

    (1998)
  • M.P. Davidson

    Chemical preservatives and natural antimicrobial compounds

  • W. Dobrogosz et al.

    Lactobacillus reuteri and enterimicrobita

    Microbial Ecology and Health and Disease

    (1989)
  • R.G. Earnshaw

    The antimicrobial action of lactic acid bacteria: Natural food preservation systems

  • Effat, B. A. (2000). Antifungal substances from some lactic acid bacteria and proprionibacteria for use as food...
  • B.A. Effat et al.

    Comparison of antifungal activity of metabolites from Lactobacillus rhamnosus, Pediococcus acidilactici and Propionibacterium thoenii

    Egyptian Journal of Dairy Sciences

    (2001)
  • T. Eklund

    Organic acid and esters

  • H.S. El-Nezami et al.

    Removal of common Fusarium toxins in vitro by strains of Lactobacillus and Propionibacterium

    Food Additives and Contaminants

    (2002)
  • Cited by (0)

    View full text